Effects of Ecology on the Gastrointestinal Parasites of Alouatta pigra

We examined the effects of demographic and ecological variables on the prevalence of intestinal parasites in free-ranging black howlers, Alouatta pigra, from Belize and Mexico. We collected 253 fecal samples from 50 individually identified monkeys during 2003. We processed all samples via standard centrifugation concentration techniques with sugar and zinc sulfate as flotation media. We used antigen capture enzyme-linked immunosorbent assays to detect protozoa. We analyzed data for each season separately. The most important factor in predicting whether an Alouatta pigra would be infected with a parasite was its membership in a particular social troop. It was not possible to isolate the effects of human presence, forest fragmentation, primate density, and the absence of Ateles geoffroyi on the prevalence of parasites in Alouatta pigra because the factors covaried. We detected few species of gastrointestinal parasites, possibly due to Alouatta pigra’s arboreal and herbivorous lifestyle and small geographic range. The prevalence of each parasite had a different pattern, with Controrchis sp. (presumed to be C. biliophilus), a fluke, tending to be more prevalent in Alouatta pigra that inhabited disturbed habitats, and Trypanoxyuris minutus, a pinworm, tending to be more prevalent in primates from undisturbed habitats. Giardia sp. tended to be more prevalent in primates at high densities. These results indicated that it is important to examine each parasite’s infection pattern separately to obtain a more accurate representation of the dynamics among the host, parasites, and ecology.     

Seroprevalence of Trypanosoma cruzi and Leishmania mexicana in Free‐Ranging Howler Monkeys in Southeastern Mexico

Natural infection of wild mammals by protozoa parasites is quite common in nature. For Neotropical Primates different infections of parasites that are etiological agent of disease in human have been identified. In particular, infections by Trypanosoma cruzi and Leishmania sp., have been reported for some New World primate species, but there are no reports of infection with these parasites in any primate species in Mexico. A serological study was conducted on two howler monkey species (Alouatta pigra and A. palliata) from the Mexican states of Campeche and Tabasco. A total of 55 serum samples (20 samples from A. pigra, 20 samples from A. palliata, and 15 samples from semifree ranging A. palliata of Los Tuxtlas, Veracruz as negative controls) were analyzed for the detection of immunoglobulin G antibodies against T. cruzi and Leishmania mexicana through enzyme linked immunosorbent assay test, indirect immunofluorescence assay and Western blot. The overall prevalence of antibodies in howler monkeys was 17.5% for T. cruzi and 30% for L. mexicana. Our results also indicate that A. pigra is more susceptible to develop leishmaniasis than A. palliata. Finally, the finding of positive serology in these primates should be given serious consideration for public health, given the potential role of these primate species as wild reservoirs for these diseases and the increasing contact of monkeys with human populations due to habitat loss and fragmentation. Am. J. Primatol. 75:161‐169, 2013. © 2012 Wiley Periodicals, Inc.     

Survey of Helminth Parasites in Populations of <Emphasis Type="Italic">Alouatta palliata mexicana</Emphasis> and <Emphasis Type="Italic">A. pigra</Emphasis> in Continuous and in Fragmented Habitat in Southern Mexico

The 2 howler species that occur in southern Mexico, Alouatta palliata mexicana and Alouatta pigra are endangered, mainly as a result of habitat loss and fragmentation from human activity. Little is known about the gastrointestinal parasite communities affecting their populations, and lack of baseline information for populations of howler species in continuous forest habitats, makes evaluations of gastrointestinal parasite prevalence in populations in fragmented landscapes difficult. We report the results of a one-time broad survey of gastrointestinal parasites in fecal samples of individuals from several demographically stable populations of Alouatta palliata mexicana and A. pigra existing in continuous and/or protected forests. We further report similar data for populations of both species in human-fragmented landscapes. We detected 6 parasites for each howler monkey species, but only 3 of them (Trematode I, Controrchis biliophilus, Trypanoxyuris sp.) were common to both species. While parasitic prevalence in populations of both howler species was, in general, higher in the fragmented habitat than in continuous and/or protected forests. The difference is only marginally significant in Alouatta pigra. Some parasites (Coccidia and Strongylid) only appeared in populations in fragmented landscapes. Preliminary data suggest that adult males tended to have higher parasite prevalence values than those of adult females in both howler species. Parasite prevalence is associated to average group size, but not to population density in Alouatta pigra.     

Potential distribution of Mexican primates: modeling the ecological niche with the maximum entropy algorithm

We developed a potential distribution model for the tropical rain forest species of primates of southern Mexico: the black howler monkey (Alouatta pigra), the mantled howler monkey (Alouatta palliata), and the spider monkey (Ateles geoffroyi). To do so, we applied the maximum entropy algorithm from the ecological niche modeling program MaxEnt. For each species, we used occurrence records from scientific collections, and published and unpublished sources, and we also used the 19 environmental coverage variables related to precipitation and temperature from WorldClim to develop the models. The predicted distribution of A. pigra was strongly associated with the mean temperature of the warmest quarter (23.6%), whereas the potential distributions of A. palliata and A. geoffroyi were strongly associated with precipitation during the coldest quarter (52.2 and 34.3% respectively). The potential distribution of A. geoffroyi is broader than that of the Alouatta spp. The areas with the greatest probability of presence of A. pigra and A. palliata are strongly associated with riparian vegetation, whereas the presence of A. geoffroyi is more strongly associated with the presence of rain forest. Our most significant contribution is the identification of areas with a high probability of the presence of these primate species, which is information that can be applied to planning future studies and then establishing criteria for the creation of areas to primate conservation in Mexico.     

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λ_max) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λ_max) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M–L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L–M hybrid sequences in A. pigra. The λ_max values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy.     

Gastrointestinal parasites of Howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Santa Marta mountain range,Veracruz, Mexico

In recent years populations of howler monkeys (Alouatta palliata) in southeastern Mexico have decreased substantially due to the transformation and loss of natural habitats. This is especially evident in the Santa Marta mountain range, Veracruz, Mexico where several studies have evaluated the impact of fragmentation on howler monkey populations in order to propose management programs for their conservation. The conditions generated by fragmentation likely change the rates of parasitic infection and could decrease howler survival. In this study, gastrointestinal parasite species richness, prevalence, and egg density of infection were determined in howler groups inhabiting five forest fragments at the Santa Marta mountain range. Two hundred and seventy‐eight fresh fecal samples were collected between October 2002 and April 2003. Three parasite species were found during the dry and the wet season in all forest fragments sampled: one unidentified species of Eimeriidae; Trypanoxyuris minutus (Oxyuridae); and Controrchis biliophilus (Dicrocoeliidae). Both the prevalence of T. minutus and infection density for all parasites differed between seasons and fragments (the largest fragment consistently differed from other fragments). Host density, distance to the nearest town, fragment size, fragment shape, and total basal area of food trees explained parasite prevalence, but each species had a different pattern. Although parasite richness was lower, prevalence and density were higher than values reported for howlers in conserved forests. These results suggest that the establishment of biological corridors and animal translocation programs must take into account the parasite ecology of each fragment to avoid higher infection rates and preclude potential consequent mortality. Am. J. Primatol. 72:539–548, 2010. © 2010 Wiley‐Liss, Inc.     

Species status of the black howler monkey,Alouatta pigra,of Belize

Small troop sizes which averaged 5.23 members per troop and the early descent of male testes inAlouatta pigra show a marked difference fromA. palliata. These differences strengthenSmith's (1970) observations of morphological differences betweenA. pigra andA. palliata.     

Geographical distribution of the black howler (Alouatta pigra) in Central America

The geographic range of the black howler,Alouatta pigra in Mexico, Guatemala, and Belize was investigated by travelling through and visiting 65 locations within or close to the expected range. The existence of the species was noted through first hand observations or was documented by talking with residents and knowledgeable people in the area. Observations were made on captive animals as well. All sites and probable sites ofA. pigra were noted to be under 1,300 ft in altitude and in areas with a mean annual temperature above 25°C and a mean annual rainfall over 1,000 mm per year. This area coincides with tropical rain forest areas, including both tropical evergreen and semievergreen rain forests.A. pigra was most plentiful in riverine areas which showed flooding for some part of the year. Two areas of possible sympatry withA. palliata were noted. In all cases, the troop sizes ofA. pigra were extremely small, under ten individuals, and infants could easily be sexed, in contrast toA. palliata which is known to occur in troops of 15–18 and is difficult to sex at an early age. Finally, a very gross method for population estimation from searching time emerged from the study.     

Necropsies disclose a low helminth parasite diversity in periurban howler monkeys

Primate–parasite interactions are often investigated via coprological studies given ethical and conservation restrictions of collecting primate hosts. Yet, these studies are inadequate to recover adult helminths for taxonomic identification and to accurately assess their prevalence, intensity, abundance, and site of infection. Fresh carcasses found in anthropogenic landscapes come as informative and reliable alternatives. In this study, we identified the helminths of brown howler monkeys (Alouatta guariba clamitans) and their sites of infection, and measured their prevalence, intensity, and abundance of infection. We necropsied 18 adult males, 11 adult females, and 7 juvenile males that died in conflicts with the anthropogenic environment (domestic dog attacks, n = 11; electrocutions and road-kills, n = 10 each; unknown, n = 5) in periurban landscapes of southern Brazil between 2013 and 2019. We found three nematodes (Trypanoxyuris minutus, Dipetalonema gracile, and Parabronema bonnei) and one cestode (Bertiella cf. studeri), a diversity estimated to account for a sampling completeness of 99%. Prevalence ranged from 3% for P. bonnei to 100% for T. minutus. Mean abundance ranged from 2 (D. gracile and B. cf. studeri) to 55,116 (T. minutus) and mean intensity of infection ranged from 4 (B. cf. studeri) to 55,116 (T. minutus). Trypanoxyuris minutus sex ratio was strongly male-biased. The intensity of infection with T. minutus was higher in juvenile males and adult females than in adult males. The low parasite diversity and the helminths' mode of transmission are compatible with howlers' arboreality and folivorous-frugivorous diet. The howlers were not infected with soil-transmitted helminth parasites of humans and domestic animals on the ground and probably did not eat invertebrates to complement the diet. Given the lack of evidence of howler health problems, we suggest that the causes of death of the necropsied howlers are the major threats to the long-term conservation of the species at the study periurban landscapes.     

Interspecific interaction and predator avoidance behavior in response to tayra (<Emphasis Type="Italic">Eira barbara</Emphasis>) by mantled howler monkeys (<Emphasis Type="Italic">Alouatta palliata</Emphasis>)

This paper reports the response of one howler monkey group (Alouatta palliata) to a group of potential predators, the tayra (Eira barbara). The apparently successful predator avoidance behavior of the monkeys was recorded in detail. We observed a group of four adult tayras moving around theAlouatta group displaying a species-typical aggressive behavioral pattern. The two adult females of the howler group successfully chased the tayras away by repeatedly moving closer to the mustelids and even following them until the predators moved off.     

Diet and activity in black howler monkeys (<Emphasis Type="Italic">Alouatta pigra</Emphasis>) in southern Belize: does degree of frugivory influence activity level?

This study reports on the diet and activity budgets of Central American black howling monkeys (Alouatta pigra) at Monkey River, Belize. This is a previously unstudied population, close to the southern boundary of the species range, and it provides comparative data on A. pigra from a new study site. Both diet and activity are within the ranges reported for other A.pigra sites and for mantled howlers (A. palliata). No age-sex differences could be discerned in either diet or activity, though monthly variation was apparent. The monkeys switch from consuming leaves 86% of the time in January to March to consuming 67% fruit in April to July. This difference was statistically significant, and provided the opportunity to compare activity levels of the monkeys over two dietary periods, one characterized primarily by folivory, the other by frugivory. Howlers are often seen as a relatively inactive species, something that is associated with a low quality, folivorous diet. However, A. pigra have been described as being as frugivorous as possible and as folivorous as necessary. Yet, despite the opportunistic consumption of large quantities of high-energy foods, A. pigra has been observed as conforming to the howler lifestyle, resting as much as 80% of the day. The data in this paper support both of these reports. Black howlers at Monkey River Belize are typically inactive, maintaining high levels of inactivity even during months characterized by frugivory, suggesting that diet is more flexible and varied than is behavior and calling into question the assumption that howler inactivity is due to the digestion of large quantities of leaves.     

Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica

In primate populations, endoparasite species richness and prevalence are associated with host traits such as reproductive and social status, age, sex, host population density, and environmental factors such as humidity. We analyzed the species richness and prevalence of intestinal parasites in two sympatric primate populations, one of Alouatta palliata and one of Ateles geoffroyi, found in a tropical dry forest in Costa Rica. We identified three species of intestinal parasites (Controrchis sp., Trypanoxyuris sp., and Strongyloides sp.) in these two primate species. We did not find any differences in species richness between the primate species. However, the prevalences of Controrchis sp. and Trypanoxyuris sp. were higher in Alouatta palliata. Similarly, males and lactating females of Alouatta palliata showed higher Controrchis sp. prevalences. We did not observe any differences in parasite richness and prevalence between seasons. Infectious diseases in endangered primate populations must be considered in conservation strategies, especially when defining protected areas.     

Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama

Habitat fragmentation may influence genetic variability through reductions in population size and the physical isolation of conspecifics. We explored the effects of these factors on genetic diversity in a population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island (BCI), Panama. The study population was established in 1914 when an unknown number of resident individuals were isolated from the surrounding mainland by damming of the Río Chagres to create the Panama Canal. Analyses of 10 microsatellite loci indicated that, despite this isolation, the howler monkeys on BCI exhibit levels of genetic diversity (H _S = 0.584 ± 0.063) among the highest reported for any species of Alouatta. These data also revealed that although relatedness among adults in a social group was significantly greater than zero, the BCI population is not highly genetically structured. Tests for genetic bottlenecks based on departures from equilibrium expectations failed to reveal evidence of a recent reduction in population size. In contrast, coalescent modeling indicated that this population has likely experienced a marked decline within the last few 100 years. These findings generate new insights into the genetic structure of A. palliata and suggest that while the formation of BCI may not have substantially reduced genetic variation in these animals, genetic diversity has been influenced by historical changes in population size.     

Male parental behavior in black howler monkeys (Alouatta palliata pigra) in Belize and Guatemala

Male parental behavior was observed in black howler monkeys (Alouatta palliata pigra) in Belize and Guatemala from December 1978 to March 1979, with the objective of relating parental behavior to the prevailing monogamous group structure. The results revealed that male parental behavior inAlouatta palliata pigra agrees in some respects with reports from the literature on polygamous and polygynous species ofAlouatta, while in other respects the situation more closely resembles that in monogamous species of non-human primates. Considerable inter-individual variability in male-infant interactions prevailed among the study groups. Male parental behavior in the Belize groups became more prominent with increasing age of an infant.     

Breeding behaviors in the black howler monkey (Alouatta pigra) of belize

Adulterous breeding between a female howling monkey (Alouatta pigra) of one troop with a male of an adjacent troop occurred despite territorial defense between the two troops. The specific behaviors are described as well as a synopsis of daily events which occurred between the female and two males from adjacent troops. A discussion of how this interaction and the behavior patterns relate to what is known about breeding in howler monkeys and related species follows.     

Artificial nest predation by brown howler monkeys (Alouatta guariba clamitans)

Howler monkeys (Alouatta spp.) have long been considered strongly vegetarian primates. Their occasional ingestion of invertebrates has largely been interpreted as unintentional. Recent observations of the consumption of bird eggs by Alouatta caraya living in small and resource-impoverished habitat patches in the state of Rio Grande do Sul (RS), Brazil help to confirm that such behavior by howler monkeys is at times intentional. We report the findings of an experimental study on artificial nest predation by free-ranging Alouatta guariba clamitans in RS and third-party unpublished observations of intentional feeding on animal matter by Alouatta arctoidea in Venezuela and Alouatta palliata in Mexico. A nest station composed of ten artificial nests baited daily with two quail eggs each was placed at six study sites. Each site was monitored from dawn to dusk during 10–12 consecutive days. Individuals (juvenile males and an adult female) from two of the six study groups inspected the nests and ate eggs once. Study subjects from these two groups were the only ones to be supplemented with food (basically fruit) by local inhabitants, a habit that may have decreased their level of neophobia and facilitated their visit to the artificial nests. We suggest that faunivory is an opportunistic and infrequent, but intentional howler monkey feeding behavior.     

Does home range use explain the relationship between group size and parasitism? A test with two sympatric species of howler monkeys

Group size is related to parasite infections in primates. This relationship probably reflects the fact that group size is associated with body contact between group members and with contact with contaminated items in the environment. The latter is highly associated with range use. In the present study we hypothesized that if infection by directly transmitted parasites (DTP) is mainly determined by the exposure of individuals to parasites that accumulate in the environment, and group size correlates negatively with the intensity of home range use, then smaller groups should be more infected by DTP. Additionally, groups that share a higher proportion of their home range with other groups should be more infected. To test our hypothesis we observed and collected fecal samples of two groups of Alouatta palliata (large group size) and two groups of A. pigra (small group size) that live sympatrically in a forest fragment located in Macuspana (Mexico). Group size was positively correlated with range area size and negatively correlated with the intensity of home range use. Range use variables were not related to either DTP prevalence or load. However, there were significant differences in DTP loads between groups, which were positively correlated with group size. Our results suggest that the intensity of home range use is a poor predictor of DTP infection parameters in groups with marked differences in size. Therefore, it is possible that the individual or combined effects of other ecological (e.g., microclimate), social (e.g., contact rate), or physiological (e.g., immune function) factors are more important in the dynamics of DTP in free-ranging primates.     

Tree-rubbing behavior of a solitary male howler monkey

On Barro Colorado Island, Panama, a solitary male howler monkey (Alouatta palliata) was observed copulating with a female member of a troop. A unique tree-rubbing behavior was then performed by the male. Within two weeks he was the dominant male in that troop.     

Free-ranging black howler monkeys, Alouatta pigra, in southern Belize are not parasitized by Controrchis biliophilus

Several coprological studies of Alouatta pigra, the black howler monkey, inhabiting Belize and Mexico have been published in the past several years. Trematodes, specifically Controrchis biliophilus (Dicrocoeliidae), have been detected in A. pigra from all locations in Belize and Mexico examined in those studies. A routine coprological survey of A. pigra was conducted in May and June 2010 as part of baseline data collection for an A. pigra population in Punta Gorda, Toledo District, southern Belize. The 51 fecal samples collected in this area were all negative for C. biliophilus. Subsequently, two additional fecal samples were collected from another population of A. pigra in Toledo District and 25 additional fecal samples were collected from six other areas of Belize during December 2010 and January 2011 and were examined for parasites. To date, C. biliophilus eggs have been detected in fecal samples from A. pigra inhabiting every district of Belize except Toledo District in southern Belize. This finding is notable, for no other population of A. pigra completely free of C. biliophilus infection had been located prior to this study.     

Chasing behavior between males within a howler monkey troop

On Barro Colorado Island, Panama, a mature male howler monkey (Alouatta palliata) was observed chasing a young adult male howler, both members of the same troop. Detailed observations on births, deaths and solitary males before and after the chase suggest a strong correlation between an unstable social structure within the troop and overt aggression between different-aged males. Support for this field work was received from the Environmental Sciences Program, Smithsonian Institution; and the National Zoological Park, Washington, D.C.